Mimicking bone extracellular matrix: Integrin-binding peptidomimetics enhance osteoblast-like cells adhesion, proliferation, and differentiation on titanium

Colloids and Surfaces B: Biointerfaces

Volumn 128, Issue , 2015, Pages 191-200

  Fraioli, Roberta ^a,b   Rechenmacher, Florian ^c   Neubauer, Stefanie ^c   Manero, José M ^a,b   Gil, Javier ^a,b   Kessler, Horst ^c,d   Mas Moruno, Carlos ^a,b  

^a UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Functionalization; Integrins; Osteointegration; Peptidomimetics; Titanium

Indexed keywords

BIOACTIVITY; BIOMIMETICS; BONE; CELL ADHESION; CELL PROLIFERATION; CONTACT ANGLE; GLYCOPROTEINS; IMPLANTS (SURGICAL); MOLECULES; PHOSPHATASES; TISSUE; TISSUE REGENERATION; TITANIUM; TITANIUM METALLOGRAPHY; X RAY PHOTOELECTRON SPECTROSCOPY;

ALKALINE PHOSPHATASE ACTIVITY; EXTRACELLULAR MATRICES; EXTRACELLULAR MATRIX PROTEIN; FUNCTIONALIZATIONS; INTEGRINS; OSTEOINTEGRATION; PEPTIDOMIMETICS; STRUCTURAL REQUIREMENTS;

CELLS;

ALKALINE PHOSPHATASE; BIOLOGICAL MARKER; BIOMATERIAL; INTEGRIN ALPHAVBETA1; PEPTIDOMIMETIC AGENT; PROTEIN BINDING; SCLEROPROTEIN; TITANIUM; TOOTH IMPLANT; VITRONECTIN RECEPTOR;

BONE; CELL ADHESION; CELL LINE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; OSTEOBLAST; SURFACE PROPERTY; SYNTHESIS; TOOTH IMPLANT;

ALKALINE PHOSPHATASE; BIOMARKERS; BONE AND BONES; CELL ADHESION; CELL LINE; CELL PROLIFERATION; COATED MATERIALS, BIOCOMPATIBLE; DENTAL IMPLANTS; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION; HUMANS; INTEGRIN ALPHAVBETA3; OSTEOBLASTS; PEPTIDOMIMETICS; PROTEIN BINDING; RECEPTORS, VITRONECTIN; SURFACE PROPERTIES; TITANIUM;

EID: 84940001297     PISSN: 09277765     EISSN: 18734367     Source Type: Journal    
DOI: 10.1016/j.colsurfb.2014.12.057     Document Type: Article

References (80)

1. Tejero R., Anitua E., Orive G. Toward the biomimetic implant surface: biopolymers on titanium-based implants for bone regeneration. Prog. Polym. Sci. 2014, 39:1406-1447. 10.1016/j.progpolymsci.2014.01.001.
2. Geetha M., Singh A.K., Asokamani R., Gogia A.K. Ti based biomaterials, the ultimate choice for orthopaedic implants - a review. Prog. Mater. Sci. 2009, 54:397-425. 10.1016/j.pmatsci.2008.06.004.
3. Anselme K., Bigerelle M. Topography effects of pure titanium substrates on human osteoblast long-term adhesion. Acta Biomater. 2005, 1:211-222. 10.1016/j.actbio.2004.11.009.
4. Wennerberg A., Albrektsson T. Effects of titanium surface topography on bone integration: a systematic review. Clin. Oral Implants Res. 2009, 20(Suppl. 4):172-184. 10.1111/j.1600-0501.2009.01775.x.
5. Nikkhah M., Edalat F., Manoucheri S., Khademhosseini A. Engineering microscale topographies to control the cell-substrate interface. Biomaterials 2012, 33:5230-5246. 10.1016/j.biomaterials.2012.03.079.
6. Kim H., Miyaji F., Kokubo T., Nakamura T. Preparation of bioactive Ti and its alloys via simple chemical surface treatment. J. Biomed. Mater. Res. 1996, 32:409-417. http://onlinelibrary.wiley.com/doi/10.1002/(SICI)1097-4636(199611)32:3%3C409::AID-JBM14%3E3.0.CO;2-B/full.
7. Kokubo T., Kim H.M., Kawashita M., Nakamura T. Bioactive metals: preparation and properties. J. Mater. Sci. Mater. Med. 2004, 15:99-107. http://www.ncbi.nlm.nih.gov/pubmed/15330042.
8. Shekaran A., García A.J. Extracellular matrix-mimetic adhesive biomaterials for bone repair. J. Biomed. Mater. Res. A 2011, 96:261-272. 10.1002/jbm.a.32979.
9. Hirano Y., Mooney D.J. Peptide and protein presenting materials for tissue engineering. Adv. Mater. 2004, 16:17-25. 10.1002/adma.200300383.
10. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687. http://www.ncbi.nlm.nih.gov/pubmed/12297042.
11. Shattil S.J., Kim C., Ginsberg M.H. The final steps of integrin activation: the end game. Nat. Rev. Mol. Cell Biol. 2010, 11:288-300. 10.1038/nrm2871.
12. Chiu L.-H., Lai W.-F.T., Chang S.-F., Wong C.-C., Fan C.-Y., Fang C.-L., et al. The effect of type II collagen on MSC osteogenic differentiation and bone defect repair. Biomaterials 2014, 35:2680-2691. 10.1016/j.biomaterials.2013.12.005.
13. Kim I.L., Khetan S., Baker B.M., Chen C.S., Burdick J.A. Fibrous hyaluronic acid hydrogels that direct MSC chondrogenesis through mechanical and adhesive cues. Biomaterials 2013, 34:5571-5580. 10.1016/j.biomaterials.2013.04.004.
14. Hersel U., Dahmen C., Kessler H. RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 2003, 24:4385-4415. 10.1016/S0142-9612(03)00343-0.
15. Benoit D.S.W., Anseth K.S. The effect on osteoblast function of colocalized RGD and PHSRN epitopes on PEG surfaces. Biomaterials 2005, 26:5209-5220. 10.1016/j.biomaterials.2005.01.045.
16. Mas-Moruno C., Fraioli R., Albericio F., Manero J.M., Gil F.J. Novel peptide-based platform for the dual presentation of biologically active peptide motifs on biomaterials. ACS Appl. Mater. Interfaces 2014, 6:6525-6536. 10.1021/am5001213.
17. Chen X., Sevilla P., Aparicio C. Surface biofunctionalization by covalent co-immobilization of oligopeptides. Colloids Surf. B: Biointerfaces 2013, 107C:189-197. 10.1016/j.colsurfb.2013.02.005.
18. Dettin M., Conconi M., Gambaretto R., Pasquato A., Folin M., Di Bello C., et al. Novel osteoblast-adhesive peptides for dental/orthopedic biomaterials. J. Biomed. Mater. Res. 2002, 60:466-471. 10.1002/jbm.10066.
19. Dettin M., Bagno A., Gambaretto R., Iucci G., Conconi M.T., Tuccitto N., et al. Covalent surface modification of titanium oxide with different adhesive peptides: surface characterization and osteoblast-like cell adhesion. J. Biomed. Mater. Res. A 2009, 90:35-45. 10.1002/jbm.a.32064.
20. Auernheimer J., Zukowski D., Dahmen C., Kantlehner M., Enderle A., Goodman S.L., et al. Titanium implant materials with improved biocompatibility through coating with phosphonate-anchored cyclic RGD peptides. Chembiochem 2005, 6:2034-2040. 10.1002/cbic.200500031.
21. Hsiong S., Boontheekul T., Huebsch N., Mooney D.J. Cyclic arginine-glycine-aspartate peptides enhance three-dimensional stem cell osteogenic differentiation. Tissue Eng. A 2009, 15:263-272. http://online.liebertpub.com/doi/abs/10.1089/ten.tea.2007.0411.
22. Kilian K.A., Mrksich M. Directing stem cell fate by controlling the affinity and density of ligand-receptor interactions at the biomaterials interface. Angew. Chem. Int. Ed. Engl. 2012, 124:4975-4979. 10.1002/ange.201108746.
23. Mas-Moruno C., Dorfner P.M., Manzenrieder F., Neubauer S., Reuning U., Burgkart R., et al. Behavior of primary human osteoblasts on trimmed and sandblasted Ti6Al4V surfaces functionalized with integrin αvβ3-selective cyclic RGD peptides. J. Biomed. Mater. Res. A 2013, 101:87-97. 10.1002/jbm.a.34303.
24. Petrie T.A., Capadona J.R., Reyes C.D., García A.J. Integrin specificity and enhanced cellular activities associated with surfaces presenting a recombinant fibronectin fragment compared to RGD supports. Biomaterials 2006, 27:5459-5470. 10.1016/j.biomaterials.2006.06.027.
25. Petrie T.A., Raynor J.E., Reyes C.D., Burns K.L., Collard D.M., García A.J. The effect of integrin-specific bioactive coatings on tissue healing and implant osseointegration. Biomaterials 2008, 29:2849-2857. 10.1016/j.biomaterials.2008.03.036.
26. Williams D.F. The role of short synthetic adhesion peptides in regenerative medicine; the debate. Biomaterials 2011, 32:4195-4197. 10.1016/j.biomaterials.2011.02.025.
27. Sun J., Wei D., Zhu Y., Zhong M., Zuo Y., Fan H., et al. A spatial patternable macroporous hydrogel with cell-affinity domains to enhance cell spreading and differentiation. Biomaterials 2014, 35:4759-4768. 10.1016/j.biomaterials.2014.02.041.
28. Rezania A., Healy K.E. Biomimetic peptide surfaces that regulate adhesion, spreading, cytoskeletal organization, and mineralization of the matrix deposited by osteoblast-like cells. Biotechnol. Prog. 1999, 15:19-32. 10.1021/bp980083b.
29. Schliephake H., Scharnweber D. Chemical and biological functionalization of titanium for dental implants. J. Mater. Chem. 2008, 18:2404-2414. 10.1039/b715355b.
30. Collier J., Segura T. Evolving the use of peptides as components of biomaterials. Biomaterials 2011, 32:4198-4204. 10.1016/j.biomaterials.2011.02.030.
31. Marchand-Brynaert J., Detrait E., Noiset O., Boxus T., Schneider Y.J., Remacle C. Biological evaluation of RGD peptidomimetics, designed for the covalent derivatization of cell culture substrata, as potential promotors of cellular adhesion. Biomaterials 1999, 20:1773-1782. http://www.ncbi.nlm.nih.gov/pubmed/10509187.
32. Dahmen C., Auernheimer J., Meyer A., Enderle A., Goodman S.L., Kessler H. Improving implant materials by coating with nonpeptidic, highly specific integrin ligands. Angew. Chem. Int. Ed. Engl. 2004, 43:6649-6652. 10.1002/anie.200460770.
33. Rechenmacher F., Neubauer S., Polleux J., Mas-Moruno C., De Simone M., Cavalcanti-Adam E.A., et al. Functionalizing αvβ3- or α5β1-selective integrin antagonists for surface coating: a method to discriminate integrin subtypes in vitro. Angew. Chem. Int. Ed. Engl. 2013, 52:1572-1575. 10.1002/anie.201206370.
34. Rechenmacher F., Neubauer S., Mas-Moruno C., Dorfner P.M., Polleux J., Guasch J., et al. A molecular toolkit for the functionalization of titanium-based biomaterials that selectively control integrin-mediated cell adhesion. Chemistry 2013, 19:9218-9223. 10.1002/chem.201301478.
35. Gronthos S., Stewart K. Integrin expression and function on human osteoblast-like cells. J. Bone Miner. Res. 1997, 12:1190-1197. http://onlinelibrary.wiley.com/doi/10.1359/jbmr.1997.12.8.1189/full.
36. Postiglione L., Di Domenico G., Ramaglia L., Montagnani S., Salzano S., Di Meglio F., et al. Behavior of SaOS-2 cells cultured on different titanium surfaces. J. Dent. Res. 2003, 82:692-696. 10.1177/154405910308200907.
37. Morgan M.R., Byron A., Humphries M.J., Bass M.D. Giving off mixed signals - distinct functions of alpha5beta1 and alphavbeta3 integrins in regulating cell behaviour. IUBMB Life 2009, 61:731-738. 10.1002/iub.200.
38. Geiger B., Spatz J.P., Bershadsky A.D. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 2009, 10:21-33. 10.1038/nrm2593.
39. Schiller H.B., Hermann M.-R., Polleux J., Vignaud T., Zanivan S., Friedel C.C., et al. β1- and αv-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments. Nat. Cell Biol. 2013, 15:625-636. 10.1038/ncb2747.
40. Roca-Cusachs P., Gauthier N.C., Del Rio A., Sheetz M.P. Clustering of alpha(5)beta(1) integrins determines adhesion strength whereas alpha(v)beta(3) and talin enable mechanotransduction. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:16245-16250. 10.1073/pnas.0902818106.
41. Rahmouni S., Lindner A., Rechenmacher F., Neubauer S., Sobahi T.R.A., Kessler H., et al. Hydrogel micropillars with integrin selective peptidomimetic functionalized nanopatterned tops: a new tool for the measurement of cell traction forces transmitted through αvβ3- or α5β1-integrins. Adv. Mater. 2013, 25:5869-5874. 10.1002/adma.201301338.
42. Fromigué O., Brun J., Marty C., Da Nascimento S., Sonnet P., Marie P.J. Peptide-based activation of alpha5 integrin for promoting osteogenesis. J. Cell. Biochem. 2012, 113:3029-3038. 10.1002/jcb.24181.
43. Lai C.-F., Cheng S.-L. Alphavbeta integrins play an essential role in BMP-2 induction of osteoblast differentiation. J. Bone Miner. Res. 2005, 20:330-340. 10.1359/JBMR.041013.
44. Gronthos S., Simmons P.J., Graves S.E., Robey P.G. Integrin-mediated interactions between human bone marrow stromal precursor cells and the extracellular matrix. Bone 2001, 28:174-181. http://www.ncbi.nlm.nih.gov/pubmed/11182375.
45. Keselowsky B.G., Collard D.M., García A.J. Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion. J. Biomed. Mater. Res. A 2003, 66:247-259. 10.1002/jbm.a.10537.
46. Neubauer S., Rechenmacher F., Brimioulle R., Di Leva F.S., Bochen A., Sobahi T.R., et al. Pharmacophoric modifications lead to superpotent αvβ3 integrin ligands with suppressed α5β1 activity. J. Med. Chem. 2014, 57:3410-3417. http://pubs.acs.org/doi/abs/10.1021/jm500092w.
47. Zhong Z., Yin S., Liu C., Zhong Y., Zhang W., Shi D., et al. Surface energy for electroluminescent polymers and indium-tin-oxide. Appl. Surf. Sci. 2003, 207:183-189. 10.1016/S0169-4332(02)01328-4.
48. Owens D.K., Wendt R.C. Estimation of the surface free energy of polymers. J. Appl. Polym. Sci. 1969, 13:1741-1747.
49. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682. 10.1038/nmeth.2019.
50. Hanawa T. A comprehensive review of techniques for biofunctionalization of titanium. J. Periodontal Implant Sci. 2011, 41:263-272. 10.5051/jpis.2011.41.6.263.
51. Han Y., Mayer D., Offenhäusser a., Ingebrandt S. Surface activation of thin silicon oxides by wet cleaning and silanization. Thin Solid Films 2006, 510:175-180. 10.1016/j.tsf.2005.11.048.
52. Godoy-Gallardo M., Mas-Moruno C., Fernández-Calderón M.C., Pérez-Giraldo C., Manero J.M., Albericio F., et al. Covalent immobilization of hLf1-11 peptide on a titanium surface reduces bacterial adhesion and biofilm formation. Acta Biomater. 2014, 10:3522-3534. 10.1016/j.actbio.2014.03.026.
53. Bagno A., Di Bello C. Surface treatments and roughness properties of Ti-based biomaterials. J. Mater. Sci. Mater. Med. 2004, 15:935-949. 10.1023/B:JMSM.0000042679.28493.7f.
54. Xiao S.J., Textor M., Spencer N.D., Wieland M., Keller B., Sigrist H. Immobilization of the cell-adhesive peptide Arg-Gly-Asp-Cys (RGDC) on titanium surfaces by covalent chemical attachment. J. Mater. Sci. Mater. Med. 1997, 8:867-872. http://www.ncbi.nlm.nih.gov/pubmed/15348806.
55. Xiao S.-J., Textor M., Spencer N.D. Covalent attachment of cell-adhesive, (Arg-Gly-Asp) - containing peptides to titanium surfaces. Langmuir 1998, 14:5507-5516.
56. Lincks J., Boyan B.D., Blanchard C.R., Lohmann C.H., Liu Y., Cochran D.L., et al. Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition. Biomaterials 1998, 19:2219-2232. http://www.ncbi.nlm.nih.gov/pubmed/9884063.
57. Lu X., Zhao Z., Leng Y. Biomimetic calcium phosphate coatings on nitric-acid-treated titanium surfaces. Mater. Sci. Eng. C 2007, 27:700-708. 10.1016/j.msec.2006.06.030.
58. Kennedy S.B., Washburn N.R., Simon C.G., Amis E.J. Combinatorial screen of the effect of surface energy on fibronectin-mediated osteoblast adhesion, spreading and proliferation. Biomaterials 2006, 27:3817-3824. 10.1016/j.biomaterials.2006.02.044.
59. Rezania A., Johnson R., Lefkow A., Healy K. Bioactivation of metal oxide surfaces. 1. Surface characterization and cell response. Langmuir 1999, 15:6931-6939. http://pubs.acs.org/doi/abs/10.1021/la990024n.
60. Pankov R. Fibronectin at a glance. J. Cell Sci. 2002, 115:3861-3863. 10.1242/jcs.00059.
61. Wilson C.J., Clegg R.E., Leavesley D.I., Pearcy M.J. Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng. 2005, 11:1-18. 10.1089/ten.2005.11.1.
62. Thomas C.H., McFarland C.D., Jenkins M.L., Rezania A., Steele J.G., Healy K.E. The role of vitronectin in the attachment and spatial distribution of bone-derived cells on materials with patterned surface chemistry. J. Biomed. Mater. Res. 1997, 37:81-93. http://www.ncbi.nlm.nih.gov/pubmed/9335352.
63. Garcia A.J., Takagi J., Boettiger D. Two-stage activation for alpha5beta1 integrin binding to surface-adsorbed fibronectin. J. Biol. Chem. 1998, 273:34710-34715. 10.1074/jbc.273.52.34710.
64. Siebers M.C., ter Brugge P.J., Walboomers X.F., Jansen J.A. Integrins as linker proteins between osteoblasts and bone replacing materials. A critical review. Biomaterials 2005, 26:137-146. 10.1016/j.biomaterials.2004.02.021.
65. Gronowicz G., McCarthy M.B. Response of human osteoblasts to implant materials: integrin-mediated adhesion. J. Orthop. Res. 1996, 14:878-887. 10.1002/jor.1100140606.
66. Keselowsky B.G., Collard D.M., García A.J. Integrin binding specificity regulates biomaterial surface chemistry effects on cell differentiation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5953-5957. 10.1073/pnas.0407356102.
67. Danen E.H.J., Sonneveld P., Brakebusch C., Fässler R., Sonnenberg A. The fibronectin-binding integrins alpha5beta1 and alphavbeta3 differentially modulate RhoA-GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis. J. Cell Biol. 2002, 159:1071-1086. 10.1083/jcb.200205014.
68. Seger R., Krebs E.G. The MAPK signaling cascade. FASEB J. 1995, 9:726-735. http://www.fasebj.org/content/9/9/726.short.
69. Cowles E.A., Brailey L.L., Gronowicz G.A. Integrin-mediated signaling regulates AP-1 transcription factors and proliferation in osteoblasts. J. Biomed. Mater. Res. 2000, 52:725-737. http://www.ncbi.nlm.nih.gov/pubmed/11033556.
70. Martino M.M., Mochizuki M., Rothenfluh D.A., Rempel S.A., Hubbell J.A., Barker T.H. Controlling integrin specificity and stem cell differentiation in 2D and 3D environments through regulation of fibronectin domain stability. Biomaterials 2009, 30:1089-1097. 10.1016/j.biomaterials.2008.10.047.
71. Kantlehner M., Schaffner P., Finsinger D., Meyer J., Jonczyk A., Diefenbach B., et al. Surface coating with cyclic RGD peptides stimulates osteoblast adhesion and proliferation as well as bone formation. Chembiochem 2000, 1:107-114. http://www.ncbi.nlm.nih.gov/pubmed/11828404.
72. López-Garcia M., Kessler H. Stimulation of bone growth on implants by integrin ligands. Handb. Miner 2007, 109-126. Wiley-VCH, Weinheim, Germany. M. Epple, E. Bäuerlein (Eds.).
73. Ku C.-H., Pioletti D.P., Browne M., Gregson P.J. Effect of different Ti-6Al-4V surface treatments on osteoblasts behaviour. Biomaterials 2002, 23:1447-1454. http://www.ncbi.nlm.nih.gov/pubmed/11829440.
74. Shapira L., Halabi A. Behavior of two osteoblast-like cell lines cultured on machined or rough titanium surfaces. Clin. Oral Implants Res. 2009, 20:50-55. 10.1111/j. 1600-0501.2008.01594.x.
75. Klinger A., Tadir A., Halabi A., Shapira L. The effect of surface processing of titanium implants on the behavior of human osteoblast-like Saos-2 cells. Clin. Implant Dent. Relat. Res. 2011, 13:64-70. 10.1111/j. 1708-8208.2009.00177.x.
76. De Angelis E., Ravanetti F., Cacchioli A., Corradi A., Giordano C., Candiani G., et al. Attachment, proliferation and osteogenic response of osteoblast-like cells cultured on titanium treated by a novel multiphase anodic spark deposition process. J. Biomed. Mater. Res. B: Appl. Biomater. 2009, 88:280-289. 10.1002/jbm.b.31179.
77. Declercq H.A., Verbeeck R.M.H., De Ridder L.I.F.J.M., Schacht E.H., Cornelissen M.J. Calcification as an indicator of osteoinductive capacity of biomaterials in osteoblastic cell cultures. Biomaterials 2005, 26:4964-4974. 10.1016/j.biomaterials.2005.01.025.
78. Cheng S.L., Lai C.F., Blystone S.D., Avioli L.V. Bone mineralization and osteoblast differentiation are negatively modulated by integrin alpha(v)beta3. J. Bone Miner. Res. 2001, 16:277-288. 10.1359/jbmr.2001.16.2.277.
79. Schneider G.B., Zaharias R., Stanford C. Osteoblast integrin adhesion and signaling regulate mineralization. J. Dent. Res. 2001, 80:1540-1544. http://cat.inist.fr/?aModele=afficheN&cpsidt=13472617.
80. Stein G., Lian J., Owen T. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J. 1990, 4:3111-3123. http://www.fasebj.org/content/4/13/3111.short.